Abstract

Experimental and theoretical studies depict the basal ganglia as a reinforcement learning system where the dopaminergic neurons provide reinforcement error signal by modulation of their firing rate. However, the low tonic discharge rate of the dopaminergic neurons suggests that their capability to encode negative events by suppressing firing rate is limited. We recorded the activity of single neurons in the basal ganglia of two monkeys during the performance of probabilistic conditioning task with food, neutral and air-puff outcomes. In a related paper we analyzed the activity of five basal ganglia populations; here, we extend this to the low-frequency discharge (LFD) neurons of the main axis of the basal ganglia, that is, the striatal phasically active neurons (PANs), and the LFD neurons in the external segment of the globus pallidus (GPe). The licking and blinking behavior during the cue presentation epoch reveals that monkeys expected different probabilistic appetitive, neutral, and aversive outcomes. Nevertheless, the activity of single striatal and GPe neurons is more strongly modulated by expectation of reward than by expectation of the aversive event. The neural-behavioral asymmetry suggests that expectation of aversive events and rewards is differentially represented at many levels of the basal ganglia.